From motor planning to execution: a sensorimotor loop perspective.

How is an evanescent wish to move translated into a concrete action? This simple question and puzzling miracle remains a focal point of motor systems neuroscience. Where does the difficulty lie? A great deal has been known about biomechanics for quite some time. More recently, there have been significant advances in our understanding of how the spinal system is organized into modules corresponding to spinal synergies, which are fixed patterns of multimuscle recruitment. But much less is known about how the supraspinal system recruits these synergies in the correct spatiotemporal pattern to effectively control movement. We argue that what makes the problem of supraspinal control so difficult is that it emerges as a result of multiple convergent and redundant sensorimotor loops. Because these loops are convergent, multiple modes of information are mixed before being sent to the spinal system; because they are redundant, information is overlapping such that a mechanism must exist to eliminate the redundancy before the signal is sent to the spinal system. Given these complex interactions, simple correlation analyses between movement variables and neural activity are likely to render a confusing and inconsistent picture. Here, we suggest that the perspective of sensorimotor loops might help in achieving a better systems-level understanding. Furthermore, state-of-the-art techniques in neurotechnology, such as optogenetics, appear to be well suited for investigating the problem of motor control at the level of loops.

Efficacy of the immediate adipose-derived stromal vascular fraction autograft on functional sensorimotor recovery after spinal cord contusion in rats.

BACKGROUND: Spinal cord injuries (SCI) lead to functional alteration with important consequences such as motor and sensory disorders. The repair strategies developed to date remain ineffective. The adipose tissue-derived stromal vascular fraction (SVF) is composed of a cocktail of cells with trophic, pro-angiogenic and immunomodulatory effects. Numerous therapeutic benefits were shown for tissue reconstitution, peripheral neuropathy and for the improvement of neurodegenerative diseases. Here, the therapeutic efficacy of SVF on sensorimotor recovery after an acute thoracic spinal cord contusion in adult rats was determined. METHOD: Male Sprague Dawley rats (n = 45) were divided into 3 groups: SHAM (without SCI and treatment), NaCl (animals with a spinal lesion and receiving a saline injection through the dura mater) and SVF (animals with a spinal lesion and receiving a fraction of fat removed from adipocytes through the dura mater). Some animals were sacrificed 14 days after the start of the experiment to determine the inflammatory reaction by measuring the interleukin-1ß, interleukin-6 and Tumor Necrosis Factor-α in the lesion area. Other animals were followed once a week for 12 weeks to assess functional recovery (postural and locomotor activities, sensorimotor coordination). At the end of this period, spinal reflexivity (rate-dependent depression of the H-reflex) and physiological adjustments (ventilatory response to metabosensitive muscle activation following muscle fatigue) were measured with electrophysiological tools. RESULTS: Compared to non-treated animals, results indicated that the SVF reduced the endogenous inflammation and increased the behavioral recovery in treated animals. Moreover, H-reflex depression and ventilatory adjustments to muscle fatigue were found to be comparable between SHAM and SVF groups. CONCLUSION: Our results highlight the effectiveness of SVF and its high therapeutic potential to improve sensorimotor functions and to restore the segmental sensorimotor loop and the communication between supra- and sub-lesional spinal cord regions after traumatic contusion.

Recognizing the individualized sensorimotor loop of stroke patients during BMI-supported rehabilitation training based on brain functional connectivity analysis.

BACKGROUND: Electroencephalogram (EEG) based brain-machine interaction training can facilitate rehabilitation by closing the sensorimotor loop. However, it remains unclear how to evaluate whether the loop is closed, especially for stroke patients whose brain regions of motor control and sensorimotor feedback could be altered. Our hypothesis is that motor recovery depends on whether sensorimotor loop is established poststroke. This study aims to explore how to evaluate the establishment of sensorimotor loop based on the evolving neural reorganization patterns after stroke. NEW METHOD: 14 stroke patients participated in the experiment and EEG were recorded during three specific tasks: Movement Imagery (MI), Passive Movement (PM) and Movement Execution (ME). Activated brain regions correlated with movement intention expression and sensorimotor feedback were detected respectively during MI and PM. In ME, local-averaged Phase Lag Index (PLI) was analyzed to represent the functional connectivity between activated brain regions of MI and PM. RESULTS: Individualized cortical activation was found both in MI and PM. The overlapping brain activation during PM and MI did not correlate with patient's Fugl-Meyer Upper Extremity Motor Score (FMU) . However, we found that FMU of the group with higher local-averaged PLI was statistically higher than FMU of the group with lower local-averaged PLI compared with global-averaged PLI (p < 0.05). CONCLUSIONS: The findings demonstrate functional connectivity between activated brain regions of motor control and sensorimotor feedback may imply if the individualized sensorimotor loop is established poststroke. The successful formation of the closed loop can indicate stroke patients' motor recovery.

Motor and sensitive recovery after injection of a physically cross-linked PNIPAAm-g-PEG hydrogel in rat hemisectioned spinal cord.

In line with experiments showing that implanted hydrogels are promising tools, we designed and injected, after a C2 spinal cord hemisection, a thermoresponsive and thermoreversible physically cross-linked poly(N-isopropylacrylamide)-poly(ethylene glycol) copolymer in order to reduce functional deficits and provide a favorable environment to axotomized axons. Nasal olfactory ecto-mesenchymal stem cells were cultured on the hydrogel in order to verify its biocompatibility. Then, inflammatory reaction (Interleukin-1ß and 6, Tumor Necrosis Factor-α) was examined 15 days post-hydrogel injection. Functional recovery (postural and locomotor activities, muscle strength and tactile sensitivity) was assessed once a week, during 12 weeks. Finally, at 12 weeks post-injection, spinal reflexivity and ventilatory adjustments were measured, and the presence of glial cells and regenerated axons were determined in the injured area. Our results indicate that cells survived and proliferated on the hydrogel which, itself, did not induce an enhanced inflammation. Furthermore, we observed significant motor and sensitive improvements in hydrogel-injected animals. Hydrogel also induced H-reflex recovery close to control animals but no improved ventilatory adjustment to electrically-evoked isometric contractions. Finally, regrowing axons were visualized within the hydrogel with no glial cells colonization. Our results emphasize the effectiveness of our copolymer and its high therapeutic potential to repair the spinal cord after injury.

Conditioning transcranial magnetic stimulation of ventral premotor cortex shortens simple reaction time.

The ventral premotor cortex (PMv) is a key area of the sensorimotor control loop, it subtends complex motor sequences, especially when the hand is involved. However, its specific contribution to simple motor response to sensory cue is still not completely clear. To investigate the role of PMv, we used transcranial magnetic stimulation (TMS) to interfere with its function during a simple reaction time (SRT) task. We ran two experiments where participants were required to respond as fast as possible to a median nerve stimulation (go-signal), while sub-M1-threshold single pulse TMS was delivered either on left (contralateral) PMv or right (ipsilateral to sensory stimulus and motor response) PMv, 5-65 ms after the go-signal. TMS delivered on either PMv up to 25 ms after the go-signal shortened reaction time. This is the time window compatible with the arrive of sensory afferences, as if conditioning before sensory afferences arrive lower the threshold needed to release the pre-planned motor program to the primary motor cortex. This is in line with a putative PMv function of buffer of pre-planned motor program not strictly lateralized in one hemisphere.

Kick Control: Using the Attracting States Arising Within the Sensorimotor Loop of Self-Organized Robots as Motor Primitives.

Self-organized robots may develop attracting states within the sensorimotor loop, that is within the phase space of neural activity, body and environmental variables. Fixpoints, limit cycles and chaotic attractors correspond in this setting to a non-moving robot, to directed, and to irregular locomotion respectively. Short higher-order control commands may hence be used to kick the system from one self-organized attractor robustly into the basin of attraction of a different attractor, a concept termed here as kick control. The individual sensorimotor states serve in this context as highly compliant motor primitives. We study different implementations of kick control for the case of simulated and real-world wheeled robots, for which the dynamics of the distinct wheels is generated independently by local feedback loops. The feedback loops are mediated by rate-encoding neurons disposing exclusively of propriosensoric inputs in terms of projections of the actual rotational angle of the wheel. The changes of the neural activity are then transmitted into a rotational motion by a simulated transmission rod akin to the transmission rods used for steam locomotives. We find that the self-organized attractor landscape may be morphed both by higher-level control signals, in the spirit of kick control, and by interacting with the environment. Bumping against a wall destroys the limit cycle corresponding to forward motion, with the consequence that the dynamical variables are then attracted in phase space by the limit cycle corresponding to backward moving. The robot, which does not dispose of any distance or contact sensors, hence reverses direction autonomously.

Neurodynamics in the Sensorimotor Loop: Representing Behavior Relevant External Situations.

In the context of the dynamical system approach to cognition and supposing that brains or brain-like systems controlling the behavior of autonomous systems are permanently driven by their sensor signals, the paper approaches the question of neurodynamics in the sensorimotor loop in a purely formal way. This is carefully done by addressing the problem in three steps, using the time-discrete dynamics of standard neural networks and a fiber space representation for better clearness. Furthermore, concepts like meta-transients, parametric stability and dynamical forms are introduced, where meta-transients describe the effect of realistic sensor inputs, parametric stability refers to a class of sensor inputs all generating the "same type" of dynamic behavior, and a dynamical form comprises the corresponding class of parametrized dynamical systems. It is argued that dynamical forms are the essential internal representatives of behavior relevant external situations. Consequently, it is suggested that dynamical forms are the basis for a memory of these situations. Finally, based on the observation that not all brain process have a direct effect on the motor activity, a natural splitting of neurodynamics into vertical (internal) and horizontal (effective) parts is introduced.

Closed-loop Robots Driven by Short-Term Synaptic Plasticity: Emergent Explorative vs. Limit-Cycle Locomotion.

We examine the hypothesis, that short-term synaptic plasticity (STSP) may generate self-organized motor patterns. We simulated sphere-shaped autonomous robots, within the LPZRobots simulation package, containing three weights moving along orthogonal internal rods. The position of a weight is controlled by a single neuron receiving excitatory input from the sensor, measuring its actual position, and inhibitory inputs from the other two neurons. The inhibitory connections are transiently plastic, following physiologically inspired STSP-rules. We find that a wide palette of motion patterns are generated through the interaction of STSP, robot, and environment (closed-loop configuration), including various forward meandering and circular motions, together with chaotic trajectories. The observed locomotion is robust with respect to additional interactions with obstacles. In the chaotic phase the robot is seemingly engaged in actively exploring its environment. We believe that our results constitute a concept of proof that transient synaptic plasticity, as described by STSP, may potentially be important for the generation of motor commands and for the emergence of complex locomotion patterns, adapting seamlessly also to unexpected environmental feedback. We observe spontaneous and collision induced mode switchings, finding in addition, that locomotion may follow transiently limit cycles which are otherwise unstable. Regular locomotion corresponds to stable limit cycles in the sensorimotor loop, which may be characterized in turn by arbitrary angles of propagation. This degeneracy is, in our analysis, one of the drivings for the chaotic wandering observed for selected parameter settings, which is induced by the smooth diffusion of the angle of propagation.

Continuous lateral oscillations as a core mechanism for taxis in Drosophila larvae.

Taxis behaviour in Drosophila larva is thought to consist of distinct control mechanisms triggering specific actions. Here, we support a simpler hypothesis: that taxis results from direct sensory modulation of continuous lateral oscillations of the anterior body, sparing the need for 'action selection'. Our analysis of larvae motion reveals a rhythmic, continuous lateral oscillation of the anterior body, encompassing all head-sweeps, small or large, without breaking the oscillatory rhythm. Further, we show that an agent-model that embeds this hypothesis reproduces a surprising number of taxis signatures observed in larvae. Also, by coupling the sensory input to a neural oscillator in continuous time, we show that the mechanism is robust and biologically plausible. The mechanism provides a simple architecture for combining information across modalities, and explaining how learnt associations modulate taxis. We discuss the results in the light of larval neural circuitry and make testable predictions.

The Umwelt of an embodied agent--a measure-theoretic definition.

We consider a general model of the sensorimotor loop of an agent interacting with the world. This formalises Uexküll's notion of a function-circle. Here, we assume a particular causal structure, mechanistically described in terms of Markov kernels. In this generality, we define two σ-algebras of events in the world that describe two respective perspectives: (1) the perspective of an external observer, (2) the intrinsic perspective of the agent. Not all aspects of the world, seen from the external perspective, are accessible to the agent. This is expressed by the fact that the second σ-algebra is a subalgebra of the first one. We propose the smaller one as formalisation of Uexküll's Umwelt concept. We show that, under continuity and compactness assumptions, the global dynamics of the world can be simplified without changing the internal process. This simplification can serve as a minimal world model that the system must have in order to be consistent with the internal process.

Re-establishing the disrupted sensorimotor loop in deafferented and deefferented people: The case of spinal cord injuries.

Acting efficiently in the world depends on the activity of motor and somatosensory systems, the integration of which is necessary for the proper functioning of the sensorimotor loop (SL). Profound alterations of SL functioning follow spinal cord injury (SCI), a condition that brings about a disconnection of the body from the brain. Such disconnection creates a substantial deprivation of somatosensorial inputs and motor outputs. Consequent somatic deficits and motor paralysis affect the body below the lesion level. A complete restoration of normal functions of the SL cannot be expected until basic neuroscience has found a way to re-establish the interrupted neural connectivity. Meanwhile, studies should focus on the development of technical solutions for dealing with the disruption of the sensorimotor loop. This review discusses the structural and functional adaptive reorganization of the brain after SCI, and the maladaptive mechanisms that impact on the processing of body related information, which alter motor imagery strategies and EEG signals. Studies that show how residual functions (e.g. face tactile sensitivity) may help people to restore a normal body image are also reviewed. Finally, data on how brain and residual body signals may be used to improve brain computer interface systems is discussed in relation to the issue of how such systems may help SCI people to re-enter the world and interact with objects and other individuals.

Behavior control in the sensorimotor loop with short-term synaptic dynamics induced by self-regulating neurons.

The behavior and skills of living systems depend on the distributed control provided by specialized and highly recurrent neural networks. Learning and memory in these systems is mediated by a set of adaptation mechanisms, known collectively as neuronal plasticity. Translating principles of recurrent neural control and plasticity to artificial agents has seen major strides, but is usually hampered by the complex interactions between the agent's body and its environment. One of the important standing issues is for the agent to support multiple stable states of behavior, so that its behavioral repertoire matches the requirements imposed by these interactions. The agent also must have the capacity to switch between these states in time scales that are comparable to those by which sensory stimulation varies. Achieving this requires a mechanism of short-term memory that allows the neurocontroller to keep track of the recent history of its input, which finds its biological counterpart in short-term synaptic plasticity. This issue is approached here by deriving synaptic dynamics in recurrent neural networks. Neurons are introduced as self-regulating units with a rich repertoire of dynamics. They exhibit homeostatic properties for certain parameter domains, which result in a set of stable states and the required short-term memory. They can also operate as oscillators, which allow them to surpass the level of activity imposed by their homeostatic operation conditions. Neural systems endowed with the derived synaptic dynamics can be utilized for the neural behavior control of autonomous mobile agents. The resulting behavior depends also on the underlying network structure, which is either engineered or developed by evolutionary techniques. The effectiveness of these self-regulating units is demonstrated by controlling locomotion of a hexapod with 18 degrees of freedom, and obstacle-avoidance of a wheel-driven robot.